Small dendritic synapses enhance temporal coding in a model of cochlear nucleus bushy cells.

Spherical bushy cells (SBCs) in the anteroventral cochlear nucleus receive a single or very few powerful axosomatic inputs from the auditory nerve. However, SBCs are also contacted by small regular bouton synapses of the auditory nerve, located in their dendritic tree. The function of these small inputs is unknown. It was speculated that the interaction of axosomatic inputs with small dendritic inputs improved temporal precision, but direct evidence for this is missing. In a compartment model of spherical bushy cells with a stylized or realistic three-dimensional (3-D) representation of the bushy dendrite, we explored this hypothesis. Phase-locked dendritic inputs caused both tonic depolarization and a modulation of the model SBC membrane potential at the frequency of the stimulus. For plausible model parameters, dendritic inputs were subthreshold. Instead, the tonic depolarization increased the excitability of the SBC model and the modulation of the membrane potential caused a phase-dependent increase in the efficacy of the main axosomatic input. This improved response rate and entrainment for low-input frequencies and temporal precision of output at and above the characteristic frequency. A careful exploration of morphological and biophysical parameters of the bushy dendrite suggested a functional explanation for the peculiar shape of the bushy dendrite. Our model for the first time directly implied a role for the small excitatory dendritic inputs in auditory processing: they modulate the efficacy of the main input and are thus a plausible mechanism for the improvement of temporal precision and fidelity in these central auditory neurons.